Regulation of Focal Adhesion Kinase Activation, Breast Cancer Cell Motility, and Amoeboid Invasion by the RhoA Guanine Nucleotide Exchange Factor Net1

REFERENCES

• Fritz G, Brachetti C, Bahlmann F, Schmidt M, Kaina B. 2002. Rho GTPases in human breast tumours: expression and mutation analyses and correlation with clinical parameters. Br. J. Cancer 87:635–644.
   PubMed Web of Science ®Google Scholar
• Fritz G, Just I, Kaina B. 1999. Rho GTPases are over-expressed in human tumors. Int. J. Cancer 81:682–687.
   PubMed Web of Science ®Google Scholar
• Jaffe AB, Hall A. 2005. Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 21:247–269.
   PubMed Web of Science ®Google Scholar
• Wheeler AP, Ridley AJ. 2004. Why three Rho proteins? RhoA, RhoB, RhoC, and cell motility. Exp. Cell Res. 301:43–49.
   PubMed Web of Science ®Google Scholar
• Burridge K, Wennerberg K. 2004. Rho and Rac take center stage. Cell 116:167–179.
   PubMed Web of Science ®Google Scholar
• Olson MF, Sahai E. 2009. The actin cytoskeleton in cancer cell motility. Clin. Exp. Metastasis 26:273–287.
   PubMed Web of Science ®Google Scholar
• Ridley AJ. 2011. Life at the leading edge. Cell 145:1012–1022.
   PubMed Web of Science ®Google Scholar
• Friedl P, Wolf K. 2010. Plasticity of cell migration: a multiscale tuning model. J. Cell Biol. 188:11–19.
   PubMed Web of Science ®Google Scholar
• Sanz-Moreno V, Marshall CJ. 2010. The plasticity of cytoskeletal dynamics underlying neoplastic cell migration. Curr. Opin. Cell Biol. 22:690–696.
   PubMed Web of Science ®Google Scholar
• Narumiya S, Tanji M, Ishizaki T. 2009. Rho signaling, ROCK and mDia1, in transformation, metastasis and invasion. Cancer Metastasis Rev. 28:65–76.
   PubMed Web of Science ®Google Scholar
• Meller N, Merlot S, Guda C. 2005. CZH proteins: a new family of Rho-GEFs. J. Cell Sci. 118:4937–4946.
   PubMed Web of Science ®Google Scholar
• Rossman KL, Der CJ, Sondek J. 2005. GEF means go: turning on RHO GTPases with guanine nucleotide-exchange factors. Nat. Rev. Mol. Cell Biol. 6:167–180.
   PubMed Web of Science ®Google Scholar
• Chan AM, Takai S, Yamada K, Miki T. 1996. Isolation of a novel oncogene, NET1, from neuroepithelioma cells by expression cDNA cloning. Oncogene 12:1259–1266.
   PubMed Web of Science ®Google Scholar
• Alberts AS, Treisman R. 1998. Activation of RhoA and SAPK/JNK signalling pathways by the RhoA-specific exchange factor mNET1. EMBO J. 17:4075–4085.
   PubMed Web of Science ®Google Scholar
• Srougi MC, Burridge K. 2011. The nuclear guanine nucleotide exchange factors Ect2 and Net1 regulate RhoB-mediated cell death after DNA damage. PLoS One 6:e17108. doi:10.1371/journal.pone.0017108.
   PubMed Web of Science ®Google Scholar
• Qin H, Carr HS, Wu X, Muallem D, Tran NH, Frost JA. 2005. Characterization of the biochemical and transforming properties of the neuroepithelial transforming protein 1. J. Biol. Chem. 280:7603–7613.
   PubMed Web of Science ®Google Scholar
• Schmidt A, Hall A. 2002. The Rho exchange factor Net1 is regulated by nuclear sequestration. J. Biol. Chem. 277:14581–14588.
   PubMed Web of Science ®Google Scholar
• Papadimitriou E, Vasilaki E, Vorvis C, Iliopoulos D, Moustakas A, Kardassis D, Stournaras C. 2012. Differential regulation of the two RhoA-specific GEF isoforms Net1/Net1A by TGF-beta and miR-24: role in epithelial-to-mesenchymal transition. Oncogene 31:2862–2875.
   PubMed Web of Science ®Google Scholar
• Shen X, Li J, Hu PP, Waddell D, Zhang J, Wang XF. 2001. The activity of guanine exchange factor NET1 is essential for transforming growth factor-beta-mediated stress fiber formation. J. Biol. Chem. 276:15362–15368.
   PubMed Web of Science ®Google Scholar
• Carr HS, Morris CA, Menon S, Song EH, Frost JA. 2013. Rac1 controls the subcellular localization of the Rho guanine nucleotide exchange factor Net1A to regulate focal adhesion formation and cell spreading. Mol. Cell. Biol. 33:622–634.
   PubMed Web of Science ®Google Scholar
• Dutertre M, Gratadou L, Dardenne E, Germann S, Samaan S, Lidereau R, Driouch K, de la Grange P, Auboeuf D. 2010. Estrogen regulation and physiopathologic significance of alternative promoters in breast cancer. Cancer Res. 70:3760–3770.
   PubMedGoogle Scholar
• Leyden J, Murray D, Moss A, Arumuguma M, Doyle E, McEntee G, O'Keane C, Doran P, MacMathuna P. 2006. Net1 and Myeov: computationally identified mediators of gastric cancer. Br. J. Cancer 94:1204–1212.
   PubMed Web of Science ®Google Scholar
• Shen SQ, Li K, Zhu N, Nakao A. 2008. Expression and clinical significance of NET-1 and PCNA in hepatocellular carcinoma. Med. Oncol. 25:341–345.
   PubMed Web of Science ®Google Scholar
• Tu Y, Lu J, Fu J, Cao Y, Fu G, Kang R, Tian X, Wang B. 2010. Over-expression of neuroepithelial-transforming protein 1 confers poor prognosis of patients with gliomas. Jpn. J. Clin. Oncol. 40:388–394.
   PubMedGoogle Scholar
• Gilcrease MZ, Kilpatrick SK, Woodward WA, Zhou X, Nicolas MM, Corley LJ, Fuller GN, Tucker SL, Diaz LK, Buchholz TA, Frost JA. 2009. Coexpression of alpha6beta4 integrin and guanine nucleotide exchange factor Net1 identifies node-positive breast cancer patients at high risk for distant metastasis. Cancer Epidemiol. Biomarkers Prev. 18:80–86.
   PubMed Web of Science ®Google Scholar
• Murray D, Horgan G, MacMathuna P, Doran P. 2008. NET1-mediated RhoA activation facilitates lysophosphatidic acid-induced cell migration and invasion in gastric cancer. Br. J. Cancer 99:1322–1329.
   PubMed Web of Science ®Google Scholar
• Carr HS, Cai C, Keinanen K, Frost JA. 2009. Interaction of the RhoA exchange factor Net1 with Discs Large Homolog 1 protects it from proteasome mediated degradation and potentiates Net1 activity. J. Biol. Chem. 284:24269–24280.
   PubMedGoogle Scholar
• Frost JA, Xu S, Hutchison MR, Marcus S, Cobb MH. 1996. Actions of Rho family small G proteins and p21-activated protein kinases on mitogen-activated protein kinase family members. Mol. Cell. Biol. 16:3707–3713.
   PubMedGoogle Scholar
• Hooper S, Marshall JF, Sahai E. 2006. Tumor cell migration in three dimensions. Methods Enzymol. 406:625–643.
   PubMedGoogle Scholar
• Scott RW, Hooper S, Crighton D, Li A, Konig I, Munro J, Trivier E, Wickman G, Morin P, Croft DR, Dawson J, Machesky L, Anderson KI, Sahai EA, Olson MF. 2010. LIM kinases are required for invasive path generation by tumor and tumor-associated stromal cells. J. Cell Biol. 191:169–185.
   PubMed Web of Science ®Google Scholar
• Iwanicki MP, Vomastek T, Tilghman RW, Martin KH, Banerjee J, Wedegaertner PB, Parsons JT. 2008. FAK, PDZ-RhoGEF and ROCKII cooperate to regulate adhesion movement and trailing-edge retraction in fibroblasts. J. Cell Sci. 121:895–905.
   PubMedGoogle Scholar
• Amano M, Ito M, Kimura K, Fukata Y, Chihara K, Nakano T, Matsuura Y, Kaibuchi K. 1996. Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). J. Biol. Chem. 271:20246–20249.
   PubMed Web of Science ®Google Scholar
• Kimura K, Ito M, Amano M, Chihara K, Fukata Y, Nakafuku M, Yamamori B, Feng J, Nakano T, Okawa K, Iwamatsu A, Kaibuchi K. 1996. Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science 273:245–248.
   PubMed Web of Science ®Google Scholar
• Garcia-Mata R, Dubash AD, Sharek L, Carr HS, Frost JA, Burridge K. 2007. The nuclear RhoA exchange factor Net1 interacts with proteins of the Dlg family, affects their localization, and influences their tumor suppressor activity. Mol. Cell. Biol. 27:8683–8697.
   PubMedGoogle Scholar
• Worthylake RA, Lemoine S, Watson JM, Burridge K. 2001. RhoA is required for monocyte tail retraction during transendothelial migration. J. Cell Biol. 154:147–160.
   PubMed Web of Science ®Google Scholar
• Yoshinaga-Ohara N, Takahashi A, Uchiyama T, Sasada M. 2002. Spatiotemporal regulation of moesin phosphorylation and rear release by Rho and serine/threonine phosphatase during neutrophil migration. Exp. Cell Res. 278:112–122.
   PubMedGoogle Scholar
• Cohen LA, Guan JL. 2005. Mechanisms of focal adhesion kinase regulation. Curr. Cancer Drug Targets 5:629–643.
   PubMed Web of Science ®Google Scholar
• Mitra SK, Schlaepfer DD. 2006. Integrin-regulated FAK-Src signaling in normal and cancer cells. Curr. Opin. Cell Biol. 18:516–523.
   PubMed Web of Science ®Google Scholar
• Lim ST, Chen XL, Lim Y, Hanson DA, Vo TT, Howerton K, Larocque N, Fisher SJ, Schlaepfer DD, Ilic D. 2008. Nuclear FAK promotes cell proliferation and survival through FERM-enhanced p53 degradation. Mol. Cell 29:9–22.
   PubMed Web of Science ®Google Scholar
• Hildebrand JD, Schaller MD, Parsons JT. 1993. Identification of sequences required for the efficient localization of the focal adhesion kinase, pp125FAK, to cellular focal adhesions. J. Cell Biol. 123:993–1005.
   PubMed Web of Science ®Google Scholar
• Katz BZ, Miyamoto S, Teramoto H, Zohar M, Krylov D, Vinson C, Gutkind JS, Yamada KM. 2002. Direct transmembrane clustering and cytoplasmic dimerization of focal adhesion kinase initiates its tyrosine phosphorylation. Biochim. Biophys. Acta 1592:141–152.
   PubMedGoogle Scholar
• Toutant M, Costa A, Studler JM, Kadare G, Carnaud M, Girault JA. 2002. Alternative splicing controls the mechanisms of FAK autophosphorylation. Mol. Cell. Biol. 22:7731–7743.
   PubMedGoogle Scholar
• Schaller MD, Hildebrand JD, Shannon JD, Fox JW, Vines RR, Parsons JT. 1994. Autophosphorylation of the focal adhesion kinase, pp125FAK, directs SH2-dependent binding of pp60src. Mol. Cell. Biol. 14:1680–1688.
   PubMed Web of Science ®Google Scholar
• Sieg DJ, Hauck CR, Schlaepfer DD. 1999. Required role of focal adhesion kinase (FAK) for integrin-stimulated cell migration. J. Cell Sci. 112:2677–2691.
   PubMed Web of Science ®Google Scholar
• Tachibana K, Sato T, D'Avirro N, Morimoto C. 1995. Direct association of pp125FAK with paxillin, the focal adhesion-targeting mechanism of pp125FAK. J. Exp. Med. 182:1089–1099.
   PubMed Web of Science ®Google Scholar
• Dobrosotskaya IY. 2001. Identification of mNET1 as a candidate ligand for the first PDZ domain of MAGI-1. Biochem. Biophys. Res. Commun. 283:969–975.
   PubMedGoogle Scholar
• Vessichelli M, Ferravante A, Zotti T, Reale C, Scudiero I, Picariello G, Vito P, Stilo R. 2012. Neuroepithelial transforming gene 1 (Net1) binds to caspase activation and recruitment domain (CARD)- and membrane-associated guanylate kinase-like domain-containing (CARMA) proteins and regulates nuclear factor kappaB activation. J. Biol. Chem. 287:13722–13730.
   PubMedGoogle Scholar
• Sahai E, Marshall CJ. 2003. Differing modes of tumour cell invasion have distinct requirements for Rho/ROCK signalling and extracellular proteolysis. Nat. Cell Biol. 5:711–719.
   PubMed Web of Science ®Google Scholar
• Wolf K, Mazo I, Leung H, Engelke K, von Andrian UH, Deryugina EI, Strongin AY, Brocker EB, Friedl P. 2003. Compensation mechanism in tumor cell migration: mesenchymal-amoeboid transition after blocking of pericellular proteolysis. J. Cell Biol. 160:267–277.
   PubMed Web of Science ®Google Scholar
• Sanz-Moreno V, Gadea G, Ahn J, Paterson H, Marra P, Pinner S, Sahai E, Marshall CJ. 2008. Rac activation and inactivation control plasticity of tumor cell movement. Cell 135:510–523.
   PubMed Web of Science ®Google Scholar
• Jiang WG, Davies G, Martin TA, Parr C, Watkins G, Mason MD, Mansel RE. 2006. Expression of membrane type-1 matrix metalloproteinase, MT1-MMP in human breast cancer and its impact on invasiveness of breast cancer cells. Int. J. Mol. Med. 17:583–590.
   PubMed Web of Science ®Google Scholar
• Wolf K, Wu YI, Liu Y, Geiger J, Tam E, Overall C, Stack MS, Friedl P. 2007. Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nat. Cell Biol. 9:893–904.
   PubMed Web of Science ®Google Scholar
• Wang Q, Liu M, Kozasa T, Rothstein JD, Sternweis PC, Neubig RR. 2004. Thrombin and lysophosphatidic acid receptors utilize distinct rhoGEFs in prostate cancer cells. J. Biol. Chem. 279:28831–28834.
   PubMed Web of Science ®Google Scholar
• Yamada T, Ohoka Y, Kogo M, Inagaki S. 2005. Physical and functional interactions of the lysophosphatidic acid receptors with PDZ domain-containing Rho guanine nucleotide exchange factors (RhoGEFs). J. Biol. Chem. 280:19358–19363.
   PubMed Web of Science ®Google Scholar
• Chrzanowska-Wodnicka M, Burridge K. 1996. Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. J. Cell Biol. 133:1403–1415.
   PubMed Web of Science ®Google Scholar
• Lim Y, Lim ST, Tomar A, Gardel M, Bernard-Trifilo JA, Chen XL, Uryu SA, Canete-Soler R, Zhai J, Lin H, Schlaepfer WW, Nalbant P, Bokoch G, Ilic D, Waterman-Storer C, Schlaepfer DD. 2008. PyK2 and FAK connections to p190Rho guanine nucleotide exchange factor regulate RhoA activity, focal adhesion formation, and cell motility. J. Cell Biol. 180:187–203.
   PubMed Web of Science ®Google Scholar
• Zhai J, Lin H, Nie Z, Wu J, Canete-Soler R, Schlaepfer WW, Schlaepfer DD. 2003. Direct interaction of focal adhesion kinase with p190RhoGEF. J. Biol. Chem. 278:24865–24873.
   PubMed Web of Science ®Google Scholar
• Fraley SI, Feng Y, Krishnamurthy R, Kim DH, Celedon A, Longmore GD, Wirtz D. 2010. A distinctive role for focal adhesion proteins in three-dimensional cell motility. Nat. Cell Biol. 12:598–604.
   PubMed Web of Science ®Google Scholar
• Sabeh F, Shimizu-Hirota R, Weiss SJ. 2009. Protease-dependent versus -independent cancer cell invasion programs: three-dimensional amoeboid movement revisited. J. Cell Biol. 185:11–19.
   PubMed Web of Science ®Google Scholar
• Nakaya Y, Sukowati EW, Wu Y, Sheng G. 2008. RhoA and microtubule dynamics control cell-basement membrane interaction in EMT during gastrulation. Nat. Cell Biol. 10:765–775.
   PubMedGoogle Scholar